ZENON, a novel POZ kruppel-like DNA binding protein associated with differentiation and/or survival of late postmitotic neurons

Molecular and Cellular Biology

Volumn 25, Issue 5, 2005, Pages 1713-1729

  Kiefer, Hélène ^a,b   Chatail Hermitte, Fabienne ^a   Ravassard, Philippe ^a,c   Bayard, Elisa ^a   Brunet, Isabelle ^a   Mallet, Jacques ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b UNIVERSITY OF TOKYO   (Japan)

^c Ipsogen SA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DNA BINDING PROTEIN; NITROGEN; TRANSCRIPTION FACTOR; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; ZENON;

ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL MATURATION; CELL NUCLEUS; CELL SURVIVAL; CLUSTER ANALYSIS; DEVELOPMENTAL STAGE; DNA BINDING; DNA ISOLATION; DNA TRANSFECTION; E BOX ELEMENT; EMBRYO DEVELOPMENT; GENETIC SCREENING; HUMAN; HUMAN CELL; MITOSIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL TUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN INTERACTION; RAT; ZINC FINGER MOTIF;

AMINO ACID SEQUENCE; ANIMALS; BRAIN; BRAIN CHEMISTRY; CELL DIFFERENTIATION; CELL SURVIVAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; PROMOTER REGIONS (GENETICS); RATS; RNA, MESSENGER; SEQUENCE ALIGNMENT; TISSUE DISTRIBUTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TYROSINE 3-MONOOXYGENASE; ZINC FINGERS;

EID: 14044258511     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.5.1713-1729.2005     Document Type: Article

References (88)

1. Adhikary, S., K. Peukert, H. Karsunky, V. Beuger, W. Lutz, H. P. Elsasser, T. Moroy, and M. Eilers. 2003. Miz1 is required for early embryonic development during gastrulation. Mol. Cell. Biol. 23:7648-7657.
2. Albagli, O., P. Dhordain, C. Deweindt, G. Lecocq, and D. Leprince. 1995. The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ. 6:1193-1198.
3. Albagli-Curiel, O. 2003. Ambivalent role of BCL6 in cell survival and transformation. Oncogene 22:507-516.
4. Albanèse, V., N. F. Biguet, H. Kiefer, E. Bayard, J. Mallet, and R. Meloni. 2001. Quantitative effects on gene silencing by allelic variation at a tetranucleotide microsatellite. Hum. Mol. Genet. 10:1785-1792.
5. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
6. Anderson, D. J., J. F. Carnahan, A. Michelsohn, and P. H. Patterson. 1991. Antibody markers identify a common progenitor to sympathetic neurons and chromaffin cells in vivo and reveal the timing of commitment to neuronal differentiation in the sympathoadrenal lineage. J. Neurosci. 11:3507-3519.
7. Avantaggiato, V., P. P. Pandolfi, M. Ruthardt, N. Hawe, D. Acampora, P. G. Pelicci, and A. Simeone. 1995. Developmental analysis of murine promyelocyte leukemia zinc finger (PLZF) gene expression: implications for the neuromeric model of the forebrain organization. J. Neurosci. 15:4927-4942.
8. Banerjee, S. A., S. Roffler-Tarlov, M. Szabo, L. Frohman, and D. M. Chikaraishi. 1994. DNA regulatory sequences of the rat tyrosine hydroxylase gene direct correct catecnolaminergic cell-type specificity of a human growth hormone reporter in the CNS of transgenic mice causing a dwarf phenotype. Brain Res. Mol. Brain Res. 24:89-106.
9. Bardwell, V. J., and R. Treisman. 1994. The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 8:1664-1677.
10. Bertuzzi, S., F. D. Porter, A. Pitts, M. Kumar, A. Agulnick, C. Wassif, and H. Westphal. 1999. Characterization of Lhx9, a novel LIM/homeobox gene expressed by the pioneer neurons in the mouse cerebral cortex. Mech. Dev. 81:193-198.
11. Biggin, M. D., and R. Tjian. 1988. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell 53:699-711.
12. Blaiseau, P. L., A. D. Isnard, Y. Surdin-Kerjan, and D. Thomas. 1997. Met31p and Met32p, two related zinc finger proteins, are involved in transcriptional regulation of yeast sulfur amino acid metabolism. Mol. Cell. Biol. 17:3640-3648.
13. Castillo, S. O., J. S. Baffi, M. Palkovits, D. S. Goldstein, I. J. Kopin, J. Witta, M. A. Magnuson, and V. M. Nikodem. 1998. Dopamine biosynthesis is selectively abolished in substantia nigra/ventral tegmental area but not in hypothalamic neurons in mice with targeted disruption of the Nurr1 gene. Mol. Cell. Neurosci. 11:36-46.
14. Cha, X. Y., R. C. Pierce, P. W. Kalivas, and S. A. Mackler. 1997. NAC-1, a rat brain mRNA, is increased in the nucleus accumbens three weeks after chronic cocaine self-administration. J. Neurosci. 17:6864-6871.
15. Collins, T., J. R. Stone, and A. J. Williams. 2001. All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol. Cell. Biol. 21:3609-3615.
16. Cook, M., A. Gould, N. Brand, J. Davies, P. Strutt, R. Shaknovich, J. Licht, S. Waxman, Z. Chen, S. Gluecksohn-Waelsch, R. Krumlauf, and A. Zelent. 1995. Expression of the zinc-finger gene PLZF at rhombomere boundaries in the vertebrate hindbrain. Proc. Natl. Acad. Sci. USA 92:2249-2253.
17. ctn interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell. Biol. 19:3614-3623.
18. Dawson, S. J., S. O. Yoon, D. M. Chikaraishi, K. A. Lillycrop, and D. S. Latchman. 1994. The Oct-2 transcription factor represses tyrosine hydroxylase expression via a heptamer TAATGARAT-like motif in the gene promoter. Nucleic Acids Res. 22:1023-1028.
19. Dhordain, P., O. Albagli, S. Ansieau, M. H. Koken, C. Deweindt, S. Quief, D. Lantoine, A. Leutz, J. P. Kerckaert, and D. Leprince. 1995. The BTB/POZ domain targets the LAZ3/BCL6 oncoprotein to nuclear dots and mediates homomerisation in vivo. Oncogene 11:2689-2697.
20. Dumas Milne Edwards, J. B., P. Ravassard, C. Icard-Liepkalns, and J. Mallet. 1995. cDNA cloning by RT-PCR, p. 89-118. In M. J. McPherson, B. D. Hames, and G. R. Taylor (ed.), PCR2: a practical approach. IRL Press, Oxford, United Kingdom.
21. Genetta, T., D. Ruezinsky, and T. Kadesch. 1994. Displacement of an E-box-binding repressor by basic helix-loop-helix proteins: implications for B-cell specificity of the immunoglobulin heavy-chain enhancer. Mol. Cell. Biol. 14:6153-6163.
22. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
23. Giniger, E., K. Tietje, L. Y. Jan, and Y. N. Jan. 1994. lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development 120:1385-1398.
24. Goeke, S., E. A. Greene, P. K. Grant, M. A. Gates, D. Crowner, T. Aigaki, and E. Giniger. 2003. Alternative splicing of lola generates 19 transcription factors controlling axon guidance in Drosophila. Nat. Neurosci. 6:917-924.
25. Guillemot, F., L. C. Lo, J. E. Johnson, A. Auerbach, D. J. Anderson, and A. L. Joyner. 1993. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75:463-476.
26. Hargrave, M., A. Karunaratne, L. Cox, S. Wood, P. Koopman, and T. Yamada. 2000. The HMG box transcription factor gene Sox14 marks a novel subset of ventral interneurons and is regulated by sonic hedgehog. Dev. Biol. 219:142-153.
27. Henthorn, P., M. Kiledjian, and T. Kadesch. 1990. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. Science 247:467-470.
28. Hirsch, M. R., M. C. Tiveron, F. Guillemot, J. F. Brunet, and C. Goridis. 1998. Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125:599-608.
29. Howard, M., D. N. Foster, and P. Cserjesi. 1999. Expression of HAND gene products may be sufficient for the differentiation of avian neural crest-derived cells into catecholaminergic neurons in culture. Dev. Biol. 215:62-77.
30. Hua, X., C. Yokoyama, J. Wu, M. R. Briggs, M. S. Brown, J. L. Goldstein, and X. Wang. 1993. SREBP-2, a second basic-helix-loop-helix-leucine zipper protein that stimulates transcription by binding to a sterol regulatory element. Proc. Natl. Acad. Sci. USA 90:11603-11607.
31. Ido, A., Y. Miura, M. Watanabe, M. Sakai, Y. Inoue, T. Miki, T. Hashimoto, T. Morinaga, S. Nishi, and T. Tamaoki. 1996. Cloning of the cDNA encoding the mouse ATBF1 transcription factor. Gene 168:227-231.
32. Kang, S. I., W. J. Chang, S. G. Cho, and I. Y. Kim. 2003. Modification of promyelocytic leukemia zinc finger protein (PLZF) by SUMO-1 conjugation regulates its transcriptional repressor activity. J. Biol. Chem. 278:51479-51483.
33. Kaplan, J., and K. Calame. 1997. The ZiN/POZ domain of ZF5 is required for both transcriptional activation and repression. Nucleic Acids Res. 25:1108-1116.
34. Kataoka, H., T. Murayama, M. Yokode, S. Mori, H. Sano, H. Ozaki, Y. Yokota, S. Nishikawa, and T. Kita. 2000. A novel snail-related transcription factor Smuc regulates basic helix-loop-helix transcription factor activities via specific E-box motifs. Nucleic Acids Res. 28:626-633.
35. Katsani, K. R., M. A. Hajibagheri, and C. P. Verrrjzer. 1999. Co-operative DNA binding by GAGA transcription factor requires the conserved BTB/POZ domain and reorganizes promoter topology. EMBO J. 18:698-708.
36. Kim, K. S., C. H. Kim, D. Y. Hwang, H. Seo, S. Chung, S. J. Hong, J. K. Lim, T. Anderson, and O. Isacson. 2003. Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. J. Neurochem. 85:622-634.
37. Kim, K. S., M. K. Lee, J. Carroll, and T. H. Joh. 1993. Both the basal and inducible transcription of the tyrosine hydroxylase gene are dependent upon a cAMP response element. J. Biol. Chem. 268:15689-15695.
38. Kim, S. W., X. Fang, H. Ji, A. F. Paulson, J. M. Daniel, M. Ciesiolka, F. van Roy, and P. D. McCrea. 2002. Isolation and characterization of XKaiso, a transcriptional repressor that associates with the catenin Xp120(ctn) in Xenopus laevis. J. Biol. Chem. 277:8202-8208.
39. Kobayashi, A., H. Yamagiwa, H. Hoshino, A. Muto, K. Sato, M. Morita, N. Hayashi, M. Yamamoto, and K. Igarashi. 2000. A combinatorial code for gene expression generated by transcription factor Bach2 and MAZR (MAZ-related factor) through the BTB/POZ domain. Mol. Cell. Biol. 20:1733-1746.
40. Kozak, M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
41. Lazaroff, M., S. Patankar, S. O. Yoon, and D. M. Chikaraishi. 1995. The cyclic AMP response element directs tyrosine hydroxylase expression in catecholaminergic central and peripheral nervous system cell lines from transgenic mice. J. Biol. Chem. 270:21579-21589.
42. Lazaroff, M., Y. Qi, and D. M. Chikaraishi. 1998. Differentiation of a catecholaminergic CNS cell line modifies tyrosine hydroxylase transcriptional regulation. J. Neurochem. 71:51-59.
43. Lee, D. K., D. Suh, H. J. Edenberg, and M. W. Hur. 2002. POZ domain transcription factor, FBI-1, represses transcription of ADH5/FDH by interacting with the zinc finger and interfering with DNA binding activity of Sp1. J. Biol. Chem. 277:26761-26768.
44. Levitt, M., S. Spector, A. Sjoerdsma, and S. Udenfriend. 1965. Elucidation of the rate-limiting step in norepinephrine biosynthesis in the perfused guinea-pig heart. J. Pharmacol. Exp. Ther. 148:1-8.
45. Li, J. Y., M. A. English, H. J. Ball, P. L. Yeyati, S. Waxman, and J. D. Licht. 1997. Sequence-specific DNA binding and transcriptional regulation by the promyelocytic leukemia zinc finger protein. J. Biol. Chem. 272:22447-22455.
46. Lim, K. C., G. Lakshmanan, S. E. Crawford, Y. Gu, F. Grosveld, and J. D. Engel. 2000. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat. Genet. 25:209-212.
47. Liu, J., J. P. Merlie, R. D. Todd, and K. L. O'Malley. 1997. Identification of cell type-specific promoter elements associated with the rat tyrosine hydroxylase gene using transgenic founder analysis. Brain Res. Mol. Brain Res. 50:33-42.
48. Mackler, S. A., L. Korutla, X. Y. Cha, M. J. Koebbe, K. M. Fournier, M. S. Bowers, and P. W. Kalivas. 2000. NAC-1 is a brain POZ/BTB protein that can prevent cocaine-induced sensitization in the rat. J. Neurosci. 20:6210-6217.
49. Melnick, A., K. F. Ahmad, S. Arai, A. Polinger, H. Ball, K. L. Borden, G. W. Carlile, G. G. Prive, and J. D. Licht. 2000. In-depth mutational analysis of the promyelocytic leukemia zinc finger BTB/POZ domain reveals motifs and residues required for biological and transcriptional functions. Mol. Cell. Biol. 20:6550-6567.
50. Melnick, A., G. Carlile, K. F. Ahmad, C. L. Kiang, C. Corcoran, V. Bardwell, G. G. Prive, and J. D. Licht. 2002. Critical residues within the BTB domain of PLZF and Bcl-6 modulate interaction with corepressors. Mol. Cell. Biol. 22:1804-1818.
51. Meloni, R., V. Albanèse, P. Ravassard, F. Treilhou, and J. Mallet. 1998. A tetranucleotide polymorphic microsatellite, located in the first intron of the tyrosine hydroxylase gene, acts as a transcription regulatory element in vitro. Hum. Mol. Genet. 7:423-428.
52. Miaw, S. C., A. Choi, E. Yu, H. Kishikawa, and I. C. Ho. 2000. ROG, repressor of GATA, regulates the expression of cytokine genes. Immunity 12:323-333.
53. Min, N., T. H. Joh, K. S. Kim, C. Peng, and J. H. Son. 1994. 5′ upstream DNA sequence of the rat tyrosine hydroxylase gene directs high-level and tissue-specific expression to catecholaminergic neurons in the central nervous system of transgenic mice. Brain Res. Mol. Brain Res. 27:281-289.
54. Morin, X., H. Cremer, M. R. Hirsch, R. P. Kapur, C. Goridis, and J. F. Brunet. 1997. Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 18:411-423.
55. Murre, C., P. S. McCaw, H. Vaessin, M. Caudy, L. Y. Jan, Y. N. Jan, C. V. Cabrera, J. N. Buskin, S. D. Hauschka, A. B. Lassar, H. Weintraub, and D. Baltimore. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537-544.
56. Nagatsu, T., M. Levitt, and S. Udenfriend. 1964. Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. J. Biol. Chem. 239:2910-2917.
57. Numoto, M., K. Yokoro, and J. Koshi. 1999. ZF5, which is a Kruppel-type transcriptional repressor, requires the zinc finger domain for self-association. Biochem. Biophys. Res. Commun. 256:573-578.
58. Okabe, S., T. Fukuda, K. Ishibashi, S. Kojima, S. Okada, M. Hatano, M. Ebara, H. Saisho, and T. Tokuhisa. 1998. BAZF, a novel Bcl6 homolog, functions as a transcriptional repressor. Mol. Cell. Biol. 18:4235-4244.
59. Pagans, S., M. Ortiz-Lombardia, M. L. Espinas, J. Bernues, and F. Azorin. 2002. The Drosophila transcription factor tramtrack (TTK) interacts with trithorax-like (GAGA) and represses GAGA-mediated activation. Nucleic Acids Res. 30:4406-4413.
60. Pagans, S., D. Pineyro, A. Kosoy, J. Bernues, and F. Azorin. 2004. Repression by TTK69 of GAGA-mediated activation occurs in the absence of TTK69 binding to DNA and solely requires the contribution of the POZ/ BTB domain of TTK69. J. Biol. Chem. 279:9725-9732.
61. Pattyn, A., X. Morin, H. Cremer, C. Goridis, and J. F. Brunet. 1999. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366-370.
62. Pessler, F., and N. Hernandez. 2003. Flexible DNA binding of the BTB/POZ-domain protein FBI-1. J. Biol. Chem. 278:29327-29335.
63. Prokhortchouk, A., B. Hendrich, H. Jorgensen, A. Ruzov, M. Wilm, G. Georgiev, A. Bird, and E. Prokhortchouk. 2001. The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15:1613-1618.
64. Puelles, L., and C. Verney. 1998. Early neuromeric distribution of tyrosine-hydroxylase-immunoreactive neurons in human embryos. J. Comp. Neurol. 394:283-308.
65. Ravassard, P., F. Chatail, J. Mallet, and C. Icard-Liepkalns. 1997. Relax, a novel rat bHLH transcriptional regulator transiently expressed in the ventricular proliferating zone of the developing central nervous system. J. Neurosci. Res. 48:146-158.
66. Remacle, J. E., H. Kraft, W. Lerchner, G. Wuytens, C. Collart, K. Verschueren, J. C. Smith, and D. Huylebroeck. 1999. New mode of DNA binding of multi-zinc finger transcription factors: deltaEF1 family members bind with two hands to two target sites. EMBO J. 18:5073-5084.
67. Retaux, S., M. Rogard, I. Bach, V. Failli, and M. J. Besson. 1999. Lhx9: a novel LIM-homeodomain gene expressed in the developing forebrain. J. Neurosci. 19:783-793.
68. Saucedo-Cardenas, O., J. D. Quintana-Hau, W. D. Le, M. P. Smidt, J. J. Cox, F. De Mayo, J. P. Burbach, and O. M. Conneely. 1998. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. USA 95:4013-4018.
69. Schimmel, J. J., L. Crews, S. Roffler-Tarlov, and D. M. Chikaraishi. 1999. 4.5 kb of the rat tyrosine hydroxylase 5′ flanking sequence directs tissue specific expression during development and contains consensus sites for multiple transcription factors. Brain Res. Mol. Brain Res. 74:1-14.
70. Smidt, M. P., C. H. Asbreuk, J. J. Cox, H. Chen, R. L. Johnson, and J. P. Burbach. 2000. A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b. Nat. Neurosci. 3:337-341.
71. Smits, S. M., T. Ponnio, O. M. Conneely, J. P. Burbach, and M. P. Smidt. 2003. Involvement of Nurr1 in specifying the neurotransmitter identity of ventral midbrain dopaminergic neurons. Eur. J. Neurosci. 18:1731-1738.
72. Son, J. H., N. Min, and T. H. Joh. 1996. Early ontogeny of catecholaminergic cell lineage in brain and peripheral neurons monitored by tyrosine hydroxylase-lacZ transgene. Brain Res. Mol. Brain Res. 36:300-308.
73. Specht, L. A., V. M. Pickel, T. H. Joh, and D. J. Reis. 1981. Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J. Comp. Neurol. 199:233-253.
74. Specht, L. A., V. M. Pickel, T. H. Joh, and D. J. Reis. 1981. Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. II. Late ontogeny. J. Comp. Neurol. 199:255-276.
75. Tinti, C., C. Yang, H. Seo, B. Conti, C. Kim, T. H. Joh, and K. S. Kim. 1997. Structure/function relationship of the cAMP response element in tyrosine hydroxylase gene transcription. J. Biol. Chem. 272:19158-19164.
76. Trocmé, C., C. Sarkis, J. M. Hermel, R. Duchateau, S. Harrison, M. Simonneau, R. Al-Shawi, and J. Mallet. 1998. CRE and TRE sequences of the rat tyrosine hydroxylase promoter are required for TH basal expression in adult mice but not in the embryo. Eur. J. Neurosci. 10:508-521.
77. Verschueren, K., J. E. Remacle, C. Collart, H. Kraft, B. S. Baker, P. Tylzanowski, L. Nelles, G. Wuytens, M. T. Su, R. Bodmer, J. C. Smith, and D. Huylebroeck. 1999. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J. Biol. Chem. 274:20489-20498.
78. Vitalis, T., O. Cases, D. Engelkamp, C. Verney, and D. J. Price. 2000. Defect of tyrosine hydroxylase-immunoreactive neurons in the brains of mice lacking the transcription factor Pax6. J. Neurosci. 20:6501-6516.
79. Vouyiouklis, D. A., and P. J. Brophy. 1995. Microtubule-associated proteins in developing oligodendrocytes: transient expression of a MAP2c isoform in oligodendrocyte precursors. J. Neurosci. Res. 42:803-817.
80. Wang, M. M., and R. R. Reed. 1993. Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast. Nature 364:121-126.
81. Wilkins, R. C., and J. T. Lis. 1997. Dynamics of potentiation and activation: GAGA factor and its role in heat shock gene regulation. Nucleic Acids Res. 25:3963-3968.
82. Wilkinson, D. G. 1994. Whole mount in situ hybridization of vertebrate embryos, p. 75-83. In D. G. Wilkinson (ed.), In situ hybridization: a practical approach. IRL Press, Oxford, United Kingdom.
83. Wilson, T. E., T. J. Fahrner, M. Johnston, and J. Milbrandt. 1991. Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science 252:1296-1300.
84. Yang, C., H. S. Kim, H. Seo, and K. S. Kim. 1998. Identification and characterization of potential cis-regulatory elements governing transcriptional activation of the rat tyrosine hydroxylase gene. J. Neurochem. 71:1358-1368.
85. Yoon, S. O., and D. M. Chikaraishi. 1994. Isolation of two E-box binding factors that interact with the rat tyrosine hydroxylase enhancer. J. Biol. Chem. 269:18453-18462.
86. Yoon, S. O., and D. M. Chikaraishi. 1992. Tissue-specific transcription of the rat tyrosine hydroxylase gene requires synergy between an AP-1 motif and an overlapping E box-containing dyad. Neuron 9:55-67.
87. Zellmer, E., Z. Zhang, D. Greco, J. Rhodes, S. Cassel, and E. J. Lewis. 1995. A homeodomain protein selectively expressed in noradrenergic tissue regulates transcription of neurotransmitter biosynthetic genes. J. Neurosci. 15:8109-8120.
88. Zetterstrom, R. H., L. Solomin, L. Jansson, B. J. Hoffer, L. Olson, and T. Perlmann. 1997. Dopamine neuron agenesis in Nurr1-deficient mice. Science 276:248-250.